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Chaperone Proteins/Heat Shock Proteins As Anticancer Vaccines

  • Michael W. Graner
  • Emmanuel Katsanis
Part of the Cancer Drug Discovery and Development book series (CDD&D)

Abstract

The chaperone proteins, a family whose members include heat shock proteins (HSPs) and stress proteins, are among the most abundant proteins found in cells. The fundamental roles played by these proteins are so essential to cell survival that they have evolutionary origins as old as Archaebacter. Despite the long history of their existence, scientists have only recently learned of the pivotal activities possessed by chaperone proteins, leading up to their use as anticancer vaccines.

Keywords

Heat Shock Protein Molecular Chaperone Chaperone Protein Transporter Associate With Antigen Processing General Vaccine 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Hemmingsen SM, Woolford C, van der Vies SM, et al. Homologous plant and bacterial proteins chaperone oligomeric protein assembly. Nature 1988; 333:330–334.PubMedCrossRefGoogle Scholar
  2. 2.
    Ellis RJ, van der Vies SM, Hemmingsen SM. The molecular chaperone concept. Biochem Soc Symp 1989; 55:145–153.PubMedGoogle Scholar
  3. 3.
    Ellis RJ, Hemmingsen SM. Molecular chaperones: proteins essential for the biogenesis of some macromolecular structures. Trends Biochem Sci 1989; 14:339–342.PubMedCrossRefGoogle Scholar
  4. 4.
    Welch WJ. The role of heat-shock proteins as molecular chaperones. Curr Opin Cell Biol 1991; 3:1033–1038.PubMedCrossRefGoogle Scholar
  5. 5.
    Bogdanov M, Dowhan W. Lipid-assisted protein folding. J Biol Chem 1999; 274:36827–36830.PubMedCrossRefGoogle Scholar
  6. 6.
    Ritossa F. A new puffing pattern induced by temperature shock and DNP in Drosophila. Experientia 1962; 18:571–573.CrossRefGoogle Scholar
  7. 7.
    Tissieres A, Mitchell HK, Tracy UM. Protein synthesis in salivary glands of Drosophila melanogaster: relation to chromosome puffs. J Mol Biol 1974; 84:389–398.PubMedCrossRefGoogle Scholar
  8. 8.
    McKenzie SL, Henikoff S, Meselson M. Localization of RNA from heat-induced polysomes at puff sites in Drosophila melanogaster. Proc Nat! Acad Sci USA 1975; 72:1117–1121.CrossRefGoogle Scholar
  9. 9.
    Spradling A, Penman S, Pardue ML. Analysis of drosophila mRNA by in situ hybridization: sequences transcribed in normal and heat shocked cultured cells. Cell 1975; 4:395–404.PubMedCrossRefGoogle Scholar
  10. 10.
    Welch WJ, Feramisco JR. Purification of the major mammalian heat shock proteins. J Biol Chem 1982; 257:14949–14059.PubMedGoogle Scholar
  11. 11.
    Lindquist S. The heat-shock response. Annu Rev Biochem 1986; 55:1151–1191.PubMedCrossRefGoogle Scholar
  12. 12.
    Welch WJ. The mammalian heat shock (or stress) response: a cellular defense mechanism. Adv Exp Med Biol 1987; 225:287–304.PubMedGoogle Scholar
  13. 13.
    Gething MJ, Sambrook J. Protein folding in the cell. Nature 1992; 355:33–45.PubMedCrossRefGoogle Scholar
  14. 14.
    Georgopoulos C, Welch WJ. Role of the major heat shock proteins as molecular chaperones. Annu Rev Cell Biol 1993; 9:601–634.PubMedCrossRefGoogle Scholar
  15. 15.
    Hart! FU. Molecular chaperones in cellular protein folding. Nature 1996; 381:571–579.CrossRefGoogle Scholar
  16. 16.
    Zimmerman SB, Minton AP. Macromolecular crowding: biochemical, biophysical, and physiological consequences. Annu Rev Biophys Biomol Struct 1993; 22:27–65.PubMedCrossRefGoogle Scholar
  17. 17.
    Minton AP. Implications of macromolecular crowding for protein assembly. Curr Opin Struct Biol 2000; 10:34–39.PubMedCrossRefGoogle Scholar
  18. 18.
    Ellis RJ. Macromolecular crowding: an important but neglected aspect of the intracellular environment. Curr Opin Struct Biol 2001; 11:114–119.PubMedCrossRefGoogle Scholar
  19. 19.
    Thirumalai D, Lorimer GH. Chaperonin-mediated protein folding. Annu Rev Biophys Biomol Struct 2001; 30:245–269.PubMedCrossRefGoogle Scholar
  20. 20.
    Frydman J. Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu Rev Biochem 2001; 70:603–647.PubMedCrossRefGoogle Scholar
  21. 21.
    Ellgaard L, Helenius A. ER quality control: towards an understanding at the molecular level. Curr Opin Cell Biol 2001; 13:431–437.PubMedCrossRefGoogle Scholar
  22. 22.
    Young JC, Moarefi I, Hart1FU. Hsp90: a specialized but essential protein-folding tool. J Cell Biol 2001; 154:267–273.PubMedCrossRefGoogle Scholar
  23. 23.
    Lee AS. The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem Sci 2001; 26:504–510.PubMedCrossRefGoogle Scholar
  24. 24.
    Berwin B, Nicchitta CV. To find the road traveled to tumor immunity: the trafficking itineraries of molecular chaperones in antigen-presenting cells. Traffic 2001; 2:690–697.PubMedCrossRefGoogle Scholar
  25. 25.
    Naylor DJ, Hart, FU. Contribution of molecular chaperones to protein folding in the cytoplasm of prokaryotic and eukaryotic cells. Biochem Soc Symp 2001:45–68.Google Scholar
  26. 26.
    Grallert H, Buchner J. Review: a structural view of the GroE chaperone cycle. J Struct Biol 2001; 135:95–103.PubMedCrossRefGoogle Scholar
  27. 27.
    Leroux MR. Protein folding and molecular chaperones in archaea. Adv App! Microbiol 2001; 50: 219–277.CrossRefGoogle Scholar
  28. 28.
    Srivastava PK, Amato RJ. Heat shock proteins: the “Swiss Army Knife” vaccines against cancers and infectious agents. Vaccine 2001; 19:2590–2597.PubMedCrossRefGoogle Scholar
  29. 29.
    Srivastava P. Interaction of heat shock proteins with peptides and antigen presenting cells: chaperoning of the innate and adaptive immune responses. Ann Rev Immunol 2002; 20:395–425.CrossRefGoogle Scholar
  30. 30.
    Nicchitta CV. Biochemical, cell biological and immunological issues surrounding the endoplasmic reticulum chaperone GRP94/gp96. Curr Opin Immunol 1998; 10:103–109.PubMedCrossRefGoogle Scholar
  31. 31.
    Argon Y, Simen BB. GRP94, an ER chaperone with protein and peptide binding properties. Semin Cell Dev Biol 1999; 10:495–505.PubMedCrossRefGoogle Scholar
  32. 32.
    Hohfeld J, Cyr DM, Patterson C. From the cradle to the grave: molecular chaperones that may choose between folding and degradation. EMBO Reports 2001; 2:885–890.PubMedCrossRefGoogle Scholar
  33. 33.
    Anfinsen CB. Principles that govern the folding of protein chains. Science 1973; 181:223–230.PubMedCrossRefGoogle Scholar
  34. 34.
    Klein G, Sjorgen HO, Klein E, Hellstrom KE. Demonstration of resistance against methylcholanthreneinduced sarcomas in the primary autochthonous host. Cancer Res 1960; 20:1561–1572.PubMedGoogle Scholar
  35. 35.
    DeLeo AB, Jay G, Appella E, Dubois GC, Law LW, Old L. Detection of a transformation-related antigen in chemically induced sarcomas and other transformed cells of the mouse. Proc Natl Acad Sci USA 1979; 76:2420–2424.PubMedCrossRefGoogle Scholar
  36. 36.
    DuBois GC, Appella E, Law LW, DeLeo AB, Old L. Immunogenic properties of soluble cytosol fractions on Meth A sarcoma cells. Cancer Res 1980; 40:4204–4208.PubMedGoogle Scholar
  37. 37.
    DuBois GC, Appella E, Law LW, DeLeo AB, Old L. The soluble antigens of BALB/c sarcoma MethA: a relationship between a serologically defined tumor-specific surface antigen (TSSA) and the tumorassociated transplantation antigen (TATA). Transplant Proc 1981; 13:1765–1773.PubMedGoogle Scholar
  38. 38.
    Srivastava PK, Das MR. The serologically unique cell surface antigen of Zajdela ascitic hepatoma is also its tumor-associated transplantation antigen. Int J Cancer 1984; 33:417–422.PubMedCrossRefGoogle Scholar
  39. 39.
    Ullrich SJ, Robinson EA, Law LW, Willingham M, Appella E. A mouse tumor-specific transplantation antigen is a heat shock-related protein. Proc Natl Acad Sci USA 1986; 83:3121–3125.PubMedCrossRefGoogle Scholar
  40. 40.
    Srivastava PK, DeLeo AB, Old L. Tumor rejection antigens of chemically induced sarcomas of inbred mice. Proc Natl Acad Sci USA 1986; 83:3407–3411.PubMedCrossRefGoogle Scholar
  41. 41.
    Kulomaa MS, Weigel NL, Kleinsek DA, et al. Amino acid sequence of a chicken heat shock protein derived from the complementary DNA nucleotide sequence. Biochemistry 1986; 25:6244–6251.PubMedCrossRefGoogle Scholar
  42. 42.
    Sargan DR, Tsai MJ, O’Malley BW. Hsp108, a novel heat shock inducible protein of chicken. Biochemistry 1986; 25:6252–6258.PubMedCrossRefGoogle Scholar
  43. 43.
    Mazzarella RA, Green M. ERp99, an abundant, conserved glycoprotein of the endoplasmic reticulum, is homologous to the 90-kDa heat shock protein (hsp90) and the 94-kDa glucose regulated protein (GRP94). J Biol Chem 1987; 262:8875–8883.PubMedGoogle Scholar
  44. 44.
    Srivastava PK, Old U. Individually distinct transplantation antigens of chemically induced mouse tumors. Immunol Today 1988; 9:78–83.PubMedCrossRefGoogle Scholar
  45. 45.
    Maki RG, Eddy RL, Jr., Byers M, Shows TB, Srivastava PK. Mapping of the genes for human endoplasmic reticular heat shock protein gp96/grp94. Somat Cell Mol Genet 1993; 19:73–81.PubMedCrossRefGoogle Scholar
  46. 46.
    Srivastava PK. Peptide-binding heat shock proteins in the endoplasmic reticulum: role in immune response to cancer and in antigen presentation. Adv Cancer Res 1993; 62:153–177.PubMedCrossRefGoogle Scholar
  47. 47.
    Udono H, Srivastava PK. Comparison of tumor-specific immunogenicities of stress-induced proteins gp96, hsp90, and hsp70. J Immunol 1994; 152:5398–5403.PubMedGoogle Scholar
  48. 48.
    Flynn GC, Chappell TG, Rothman JE. Peptide binding and release by proteins implicated as catalysts of protein assembly. Science 1989; 245:385–390.PubMedCrossRefGoogle Scholar
  49. 49.
    Flynn GC, Pohl J, Flocco MT, Rothman JE. Peptide-binding specificity of the molecular chaperone BiP. Nature 1991; 353:726–730.PubMedCrossRefGoogle Scholar
  50. 50.
    Udono H, Srivastava PK. Heat shock protein 70-associated peptides elicit specific cancer immunity. J Exp Med 1993; 178:1391–1396.PubMedCrossRefGoogle Scholar
  51. 51.
    Ishii T, Udono H, Yamano T, et al. Isolation of MHC class I-restricted tumor antigen peptide and its precursors associated with heat shock proteins hsp70, hsp90, and gp96. J Immunol 1999; 162:1303–1309.PubMedGoogle Scholar
  52. 52.
    Castelli C, Ciupitu AM, Rini F, et al. Human heat shock protein 70 peptide complexes specifically activate antimelanoma T cells. Cancer Res 2001; 61:222–227.PubMedGoogle Scholar
  53. 53.
    Blachere NE, Udono H, Janetzki S, Li Z, Heike M, Srivastava PK. Heat shock protein vaccines against cancer. J Immunother 1993; 14:352–356.CrossRefGoogle Scholar
  54. 54.
    Suto R, Srivastava PK. A mechanism for the specific immunogenicity of heat shock protein-chaperoned peptides. Science 1995; 269:1585–1588.PubMedCrossRefGoogle Scholar
  55. 55.
    Nieland TJ, Tan MC, Monne-van Muijen M, Koning F, Kruisbeek AM, van Bleek GM. Isolation of an immunodominant viral peptide that is endogenously bound to the stress protein GP96/GRP94. Proc Nat! Acad Sei USA 1996; 93:6135–6139.CrossRefGoogle Scholar
  56. 56.
    Heikema A, Agsteribbe E, Wilschut J, Huckriede A. Generation of heat shock protein-based vaccines by intracellular b adine of gp96 with antigenic peptides. Immunol Lett 1997; 57:69–74.PubMedCrossRefGoogle Scholar
  57. 57.
    Meng SD, Gao T, Gao GF, Tien P. HBV-specific peptide associated with heat-shock protein gp96. Lancet 2001; 357:528–529.PubMedCrossRefGoogle Scholar
  58. 58.
    Arnold D, Faath S, Rammensee H, Schild H. Crosspriming of minor histocompatibility antigenspecific cytotoxic T cells upon immunization with the heat shock protein gp96. J Exp Med 1995; 182:885–889.PubMedCrossRefGoogle Scholar
  59. 59.
    Breloer M, Marti T, Fleischer B, von Bonin A. Isolation of processed, H-2Kb-binding ovalbuminderived peptides associated with the stress proteins HSP70 and gp96. Eur J Immunol 1998; 28:1016–1021.PubMedCrossRefGoogle Scholar
  60. 60.
    Nair S, Wearsch PA, Mitchell DA, Wassenberg JJ, Gilboa E, Nicchitta CV. Calreticulin displays in vivo peptide-binding activity and can elicit CTL responses against bound peptides. J Immunol 1999; 162:6426–6432.PubMedGoogle Scholar
  61. 61.
    Zhu X, Zhao X, Burkholder WF, et al. Structural analysis of substrate binding by the molecular chaperone DnaK. Science 1996; 272:1606–1614.PubMedCrossRefGoogle Scholar
  62. 62.
    Morshauser RC, Wang H, Flynn GC, Zuiderweg ER. The peptide-binding domain of the chaperone protein Hsc70 has an unusual secondary structure topology. Biochemistry 1995; 34:6261–6266.PubMedCrossRefGoogle Scholar
  63. 63.
    Peng P, Menoret A, Srivastava PK. Purification of immunogenic heat shock protein 70-peptide complexes by ADP-affinity chromatography. J Immunol Methods 1997; 204:13–21.PubMedCrossRefGoogle Scholar
  64. 64.
    Blachere NE, Li Z, Chandawarkar RY, et al. Heat shock protein-peptide complexes, reconstituted in vitro, elicit peptide-specific cytotoxic T lymphocyte response and tumor immunity. J Exp Med 1997; 186:1315–1322.PubMedCrossRefGoogle Scholar
  65. 65.
    Ciupitu AM, Petersson M, O’Donnell CL, et al. Immunization with a lymphocytic choriomeningitis virus peptide mixed with heat shock protein 70 results in protective antiviral immunity and specific cytotoxic T lymphocytes. J Exp Med 1998; 187:685–691.PubMedCrossRefGoogle Scholar
  66. 66.
    Wearsch PA, Voglino L, Nicchitta CV. Structural transitions accompanying the activation of peptide binding to the endoplasmic reticulum Hsp90 chaperone GRP94. Biochemistry 1998; 37:5709–5719.PubMedCrossRefGoogle Scholar
  67. 67.
    Srivastava PK, Udono H, Blachere NE, Li Z. Heat shock proteins transfer peptides during antigen processing and CTL priming. Immunogenetics 1994; 39:93–98.PubMedCrossRefGoogle Scholar
  68. 68.
    Rivett AJ. Intracellular distribution of proteasomes. Curr Opin Immunol 1998; 10:110–114.PubMedCrossRefGoogle Scholar
  69. 69.
    Srivastava PK, Menoret A, Basu S, Binder RJ, McQuade KL. Heat shock proteins come of age: primitive functions acquire new roles in an adaptive world. Immunity 1998; 8:657–665.PubMedCrossRefGoogle Scholar
  70. 70.
    Maeurer MJ, Gollin SM, Martin D, et al. Tumor escape from immune recognition: lethal recurrent melanoma in a patient associated with downregulation of the peptide transporter protein TAP-1 and loss of expression of the immunodominant MART-1/Melan-A antigen. J Clin Invest 1996; 98:1633–1641.PubMedCrossRefGoogle Scholar
  71. 71.
    Marincola FM, Jaffee EM, Hicklin DJ, Ferrone S. Escape of human solid tumors from T-cell recognition: molecular mechanisms and functional significance. Adv Immunol 2000; 74:181–273.PubMedCrossRefGoogle Scholar
  72. 72.
    Ohnmacht GA, Wang E, Mocellin S, et al. Short-term kinetics of tumor antigen expression in response to vaccination. J Immunol 2001; 167:1809–1820.PubMedGoogle Scholar
  73. 73.
    Graner MW, Zeng Y, Feng H, Katsanis E. Tumor-derived chaperone-rich cell lysates are effective theranentic vaccines against a variety of cancers. Cancer Immunol Immunotherapy 2003; 52:226–234.Google Scholar
  74. 74.
    Li Z. Priming of T cells by heat shock protein-peptide complexes as the basis of tumor vaccines. Semin Immunol 1997; 9:315–322.PubMedCrossRefGoogle Scholar
  75. 75.
    Graner M, Raymond A, Romney D, He L, Whitesell L, Katsanis E. Immunoprotective activities of multiple chaperone proteins isolated from murine B-cell leukemia/lymphoma. Clin Cancer Res 2000; 6:909–915.PubMedGoogle Scholar
  76. 76.
    Menoret A, Bell G. Purification of multiple heat shock proteins from a single tumor sample. J Immunol Meth 2000; 237:119–130.CrossRefGoogle Scholar
  77. 77.
    Graner M, Raymond A, Akporiaye E, Katsanis E. Tumor-derived multiple chaperone enrichment by free-solution isoelectric focusing yields potent antitumor vaccines. Cancer Immunol Immunother 2000; 49:476–484.PubMedCrossRefGoogle Scholar
  78. 78.
    Zeng Y, Feng H, Graner MW, Katsanis E. Tumor-derived chaperone-rich cell lysates activate dendritic cells and elicit potent anti-tumor immunity. Blood 2003; 101:4485–4491.PubMedCrossRefGoogle Scholar
  79. 79.
    Binder RJ, Han DK, Srivastava PK. CD91: a receptor for heat shock protein gp96. Nat Immunol 2000; 1:151–155.PubMedCrossRefGoogle Scholar
  80. 80.
    Asea A, Kraeft SK, Kurt-Jones EA, et al. HSP70 stimulates cytokine production through a CD14dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med 2000; 6:435–442.PubMedCrossRefGoogle Scholar
  81. 81.
    Basu S, Binder RJ, Ramalingam T, Srivastava PK. CD91 is a common receptor for heat shock proteins gp96, hsp90, hsp70, and calreticulin. Immunity 2001; 14:303–313.PubMedCrossRefGoogle Scholar
  82. 82.
    Binder RJ, Karimeddini D, Srivastava PK. Adjuvanticity of alpha 2-macroglobulin, an independent ligand for the heat shock protein receptor CD91. J Immunol 2001; 166:4968–4972.PubMedGoogle Scholar
  83. 83.
    Kol A, Lichtman AH, Finberg RW, Libby P, Kurt-Jones EA. Cutting edge: heat shock protein (HSP) 60 activates the innate immune response: CD14 is an essential receptor for HSP60 activation of mononuclear cells. J Immunol 2000; 164:13–17.PubMedGoogle Scholar
  84. 84.
    Ohashi K, Burkart V, Flohe S, Kolb H. Cutting edge: heat shock protein 60 is a putative endogenous ligand of the toll-like receptor-4 complex. J Immunol 2000; 164:558–561.PubMedGoogle Scholar
  85. 85.
    Vabulas RM, Braedel S, Hilf N, et al. The endoplasmic reticulum-resident heat shock protein Gp96 activates dendritic cells via the Toll-like receptor 2/4 pathway. J Biol Chem 2002; 277:20847–20853.PubMedCrossRefGoogle Scholar
  86. 86.
    Panjwani N, Popova L, Febbraio M, Srivastava PK. The CD36 scavenger receptor as a receptor for Gp96. Cell Stress Chaperones 2000; 5:391.Google Scholar
  87. 87.
    Berwin B, Hart JP, Pizzo SV, Nicchitta CV. Cutting edge: CD91-independent cross-presentation of GRP94(gp96)-associated peptides. J Immunol 2002; 168:4282–4286.PubMedGoogle Scholar
  88. 88.
    Singh-Jasuja H, Scherer HU, Hilf N, et al. The heat shock protein gp96 induces maturation of dendritic cells and down-regulation of its receptor. Eur J Immunol 2000; 30:2211–2215.PubMedGoogle Scholar
  89. 89.
    Basu S, Binder RJ, Suto R, Anderson KM, Srivastava PK. Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate the NFkappa B pathway. Int Immunol 2000; 12:1539–1546.PubMedCrossRefGoogle Scholar
  90. 90.
    Feng H, Zeng Y, Graner MW, Likhacheva A, Katsanis E. Exogenous stress proteins enhance the immunogenicity of apoptotic tumor cells and stimulate anti-tumor immunity. Blood 2003; 101:245–252.PubMedCrossRefGoogle Scholar
  91. 91.
    Matzinger P. Tolerance, danger, and the extended family. Ann Rev Immunol 1994; 12:991–1045.CrossRefGoogle Scholar
  92. 92.
    Gallucci S, Matzinger P. Danger signals: SOS to the immune system. Curr Opin Immunol 2001; 13:114–119.PubMedCrossRefGoogle Scholar
  93. 93.
    Melcher A, Todryk S, Hardwick N, Ford M, Jacobson M, Vile RG. Tumor immunogenicity is determined by the mechanism of cell death via induction of heat shock protein expression. Nat Med 1998; 4:581–587.PubMedCrossRefGoogle Scholar
  94. 94.
    Todryk S, Melcher AA, Hardwick N, et al. Heat shock protein 70 induced during tumor cell killing induces Th 1 cytokines and targets immature dendritic cell precursors to enhance antigen uptake. J Immunol 1999; 163:1398–1408.PubMedGoogle Scholar
  95. 95.
    Berwin B, Reed RC, Nicchitta CV. Virally induced lytic cell death elicits the release of immunogenic GRP94/gp96. J Biol Chem 2001; 276:21083–21088.PubMedCrossRefGoogle Scholar
  96. 96.
    Gough MJ, Melcher AA, Ahmed A, et al. Macrophages orchestrate the immune response to tumor cell death. Cancer Res 2001; 61:7240–7247.PubMedGoogle Scholar
  97. 97.
    Feng H, Zeng Y, Whitesell L, Katsanis E. Stressed apoptotic tumor cells express heat shock proteins and elicit tumor-specific immunity. Blood 2001; 97:3505–3512.PubMedCrossRefGoogle Scholar
  98. 98.
    Feng H, Zeng Y, Graner MW, Katsanis E. Stressed apoptotic tumor cells stimulate dendritic cells and induce specific cytotoxic T cells. Blood 2002; 100:4108–4115.PubMedCrossRefGoogle Scholar
  99. 99.
    Hilf N, Singh-Jasuja H, Schwarzmaier P, Gouttefangeas C, Rammensee HG, Schild H. Human platelets express heat shock protein receptors and regulate dendritic cell maturation. Blood 2002; 99:3676–3682.PubMedCrossRefGoogle Scholar
  100. 100.
    Chandawarkar RY, Wagh MS, Srivastava PK. The dual nature of specific immunological activity of tumor-derived gp96 preparations. J Exp Med 1999; 189:1437–1442.PubMedCrossRefGoogle Scholar
  101. 101.
    Janetzki S, Palla D, Rosenhauer V, Lochs H, Lewis JJ, Srivastava PK. Immunization of cancer patients with autologous cancer-derived heat shock protein gp96 preparations: a pilot study. Int J Cancer 2000; 88:232–238.PubMedCrossRefGoogle Scholar
  102. 102.
    Cancer Vaccines-Antigenics. BioDrugs 2002; 16:72–74.Google Scholar
  103. 103.
    Parmiani G, Belli F, Testori A, Maio M, Roberto M. Clinical and immunological results of vaccination with autologous heat-shock protein peptide complex-96 (HSPPC-96) in metastatic melanoma. American Society of Clinical Oncology (ASCO) Proceedings 2001; 20:1006.Google Scholar
  104. 104.
    Mazzaferro V, Coppa JC, Carrabba MG, Rivoltini L, Schiavo M, et al. Vaccination with autologous tumor derived heat shock protein peptide complex Gp-96 (HSPPC-96) following curative resection of colorectal liver metastases. American Society of Clinical Oncology (ASCO) Proceedings 2001; 20:1020.Google Scholar
  105. 105.
    Amato R, Hawkins E, Reitsma D, et al. Patients with renal cell carcinoma (RCC) using autologous tumor-derived heat shock protein-peptide complex (HSPPC-96) with or without interleukin-2 (IL-2). American Society of Clinical Oncology (ASCO) Proceedings 2000; 19:1782.Google Scholar
  106. 106.
    Hertkom C, Lehr A, Woelfel T, et al. Phase I trial of vaccination with autologous tumor-derived gp96 (oncophage) in patients after surgery for gastric cancer. American Society of Clinical Oncology (ASCO) Proceedings 2002; 21:117.Google Scholar
  107. 107.
    Murray B, Desantis D, Houghton A, et al. Pilot trial of vaccination with autologous tumor-derived gp96 heat shock protein-peptide complex (HSPPC-96) in patients with resected pancreatic adenocarcinoma. American Society of Clinical Oncology (ASCO) Proceedings 1999; 18.Google Scholar
  108. 108.
    Reed Sporn J, Laska E, Gran D, et al. Treatment of low-grade B-cell neoplasms with heat-shock proteintumor protein complex. American Society of Clinical Oncology (ASCO) Proceedings 2001; 20:2643.Google Scholar
  109. 109.
    Lindquist S, Craig EA. The heat-shock proteins. Annu Rev Genet 1988; 22:631–677.PubMedCrossRefGoogle Scholar
  110. 110.
    Lee-Yoon D, Easton D, Murawski M, Burd R, Subjeck JR. Identification of a major subfamily of large hsp70-like proteins through the cloning of the mammalian 110-kDa heat shock protein. J Biol Chem 1995; 270:15725–15733.PubMedCrossRefGoogle Scholar
  111. 111.
    Lin HY, Masso-Welch P, Di YP, Cai JW, Shen JW, Subjeck JR. The 170-kDa glucose-regulated stress protein is an endoplasmic reticulum protein that binds immunoglobulin. Mol Biol Cell 1993;4:1109–1119.PubMedGoogle Scholar
  112. 112.
    Oh HJ, Chen X, Subjeck JR. Hsp110 protects heat-denatured proteins and confers cellular thermoresistance. J Biol Chem 1997; 272:31636–31640.PubMedCrossRefGoogle Scholar
  113. 113.
    Oh HJ, Easton D, Murawski M, Kaneko Y, Subjeck JR. The chaperoning activity of hsp110. Identification of functional domains by use of targeted deletions. J Biol Chem 1999; 274:15712–15718.PubMedCrossRefGoogle Scholar
  114. 114.
    Easton DP, Kaneko Y, Subjeck JR. The hsp110 and Grpl 70 stress proteins: newly recognized relatives of the Hsp70s. Cell Stress Chaperones 2000; 5:276–290.PubMedCrossRefGoogle Scholar
  115. 115.
    Wang XY, Kazim L, Repasky EA, Subjeck JR. Characterization of heat shock protein 110 and glucoseregulated protein 170 as cancer vaccines and the effect of fever-range hyperthermia on vaccine. J Immunol 2001: 166:490–497.PubMedGoogle Scholar
  116. 116.
    Manjili MH, Henderson R, Wang XY, Chen X, Li Y, Repasky E, Kazim L, Subjeck JR. Development of a recombinant HSP110-HER-2/neu vaccine using the chaperoning properties of HSP110. Cancer Res 2002; 62:1737–1742.PubMedGoogle Scholar
  117. 117.
    Suzuki CK, Rep M, van Dijl JM, Suda K, Grivell LA, Schatz G. ATP-dependent proteases that also chaperone protein biogenesis. Trends Biochem Sci 1997; 22:118–123.PubMedCrossRefGoogle Scholar
  118. 118.
    Porankiewicz J, Wang J, Clark AK. New insights into the ATP-dependent Clp protease: Escherichia col i and beyond. Mol Microbiol 1999; 32:449–458.PubMedCrossRefGoogle Scholar
  119. 119.
    Ben-Zvi AP, Goloubinoff P. Review: mechanisms of disaggregation and refolding of stable protein aggregates by molecular chaperones. J Structural Biol 2001; 135:84–93.CrossRefGoogle Scholar
  120. 120.
    Pratt WB. The role of the hsp90-based chaperone system in signal transduction by nuclear receptors and receptors signaling via MAP kinase. Annu Rev Pharmacol Toxicol 1997; 37:297–326.PubMedCrossRefGoogle Scholar
  121. 121.
    Csermely P, Schnaider T, Soti C, Prohaszka Z, Nardai G. The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review. Pharmacol Ther 1998; 79:129–168.PubMedCrossRefGoogle Scholar
  122. 122.
    Mayer MP, Bukau B. Molecular chaperones: the busy life of Hsp90. Curr Biol 1999; 9:R322-R325.PubMedCrossRefGoogle Scholar
  123. 123.
    Queitsch C, Sangster TA, Lindquist S. Hsp90 as a capacitor of phenotypic variation. Nature 2002; 417:618–624.PubMedCrossRefGoogle Scholar
  124. 124.
    Fink AL. Chaperone-mediated protein folding. Physiol Rev 1999; 79:425–429.PubMedGoogle Scholar
  125. 125.
    Ohtsuka K, Hata M. Molecular chaperone function of mammalian Hsp70 and Hsp40-a review. Int J Hyperthermia 2000; 16:231–245.PubMedCrossRefGoogle Scholar
  126. 126.
    Winfield JB, Jarjour WN. Stress proteins, autoimmunity, and autoimmune disease. CUIT Top Microbiol Immunol 1991; 167:161–189.CrossRefGoogle Scholar
  127. 127.
    Hendrick JP, Hart FU. The role of molecular chaperones in protein folding. FASEB J 1995; 9:1559–1569.PubMedGoogle Scholar
  128. 128.
    Laad AD, Thomas ML, Fakih AR, Chiplunkar SV. Human gamma delta T cells recognize heat shock protein-60 on oral tumor cells. Int J Cancer 1998; 80:709–714.CrossRefGoogle Scholar
  129. 129.
    Thomas ML, Samant UC, Deshpande RK, Chiplunkar SV. Gammadelta T cells lyse autologous and allogenic oesophageal tumours: involvement of heat-shock proteins in the tumour cell lysis. Cancer Immunol Immunother 2000; 48:653–659.PubMedCrossRefGoogle Scholar
  130. 130.
    Barazi HO, Zhou L, Templeton NS, Krutzsch HC, Roberts DD. Identification of heat shock protein 60 as a molecular mediator of alpha 3 beta 1 integrin activation. Cancer Res 2002; 62:1541–1548.PubMedGoogle Scholar
  131. 131.
    Ciocca DR, Oesterreich S, Chamness GC, McGuire WL, Fuqua SA. Biological and clinical implications of heat shock protein 27,000 (Hsp27): a review. J Natl Cancer Inst 1993; 85:1558–1570.PubMedCrossRefGoogle Scholar
  132. 132.
    Marcario AJ. Heat-shock proteins and molecular chaperones: implications for pathogenesis, diagnostics, and therapeutics. Int J Clin Lab Res 1995; 25:59–70.CrossRefGoogle Scholar
  133. 133.
    Narberhaus F. Alpha-crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol Mol Biol Rev 2002; 66:64–93.PubMedCrossRefGoogle Scholar
  134. 134.
    Morton H, Cavanagh AC, Athanasas-Platsis S, Quinn KA, Rolfe BE. Early pregnancy factor has immunosuppressive and growth factor properties. Reprod Fertil Dey 1992; 4:411–422.CrossRefGoogle Scholar
  135. 135.
    Gupta RS. Evolution of the chaperonin families (Hsp60, Hsp10 and Tcp-1) of proteins and the origin of eukaryotic cells. Mol Microbiol 1995; 15:1–11.PubMedCrossRefGoogle Scholar
  136. 136.
    Cavanagh AC. Identification of early pregnancy factor as chaperonin 10: implications for understanding its role. Rev Reprod 1996; 1:28–32.PubMedCrossRefGoogle Scholar
  137. 137.
    Athanasas-Platsis S, Corcoran CM, Kaye PL, Cavanagh AC, Morton H. Early pregnancy factor is required at two important stages of embryonic development in the mouse. Am J Reprod Immunol 2000; 43:223–233.PubMedCrossRefGoogle Scholar
  138. 138.
    Sadacharan SK, Cavanagh AC, Gupta RS. Immunoelectron microscopy provides evidence for the presence of mitochondrial heat shock 10-kDa protein (chaperonin 10) in red blood cells and a variety of secretory granules. Histochem Cell Biol 2001; 116:507–517.PubMedCrossRefGoogle Scholar

Copyright information

© Humana Press Inc. 2004

Authors and Affiliations

  • Michael W. Graner
  • Emmanuel Katsanis

There are no affiliations available

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